Chronic psychological distress as an inducer of microglial activation and leukocyte recruitment into the area postrema

NeuroImmunoModulation

Volumn 22, Issue 5, 2015, Pages 311-321

  Vargas Caraveo, Alejandra ^a,b   Pérez Ishiwara, David Guillermo ^a   Martínez Martínez, Alejandro ^b  

^a INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

^b UNIVERSIDAD AUTÓNOMA DE CIUDAD JUÁREZ   (Mexico)

Author keywords

Area postrema; CD11b; CD45; Leukocyte recruitment; Lymphocytes; Microglial activation; Monocytes; Neuroinflammation; TrkA

Indexed keywords

CD11B ANTIGEN; CD45 ANTIGEN; PROTEIN TYROSINE KINASE A;

ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; AREA POSTREMA; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; DISTRESS SYNDROME; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; LEUKOCYTE ACTIVATION; LYMPHOCYTE; MACROPHAGE; MALE; MICROGLIA; MONOCYTE; NONHUMAN; PRIORITY JOURNAL; RAT; ANIMAL; CHRONIC DISEASE; DISEASE MODEL; FLOW CYTOMETRY; LEUKOCYTE; MACROPHAGE ACTIVATION; MENTAL STRESS; METABOLISM; PATHOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; ANTIGENS, CD11B; ANTIGENS, CD45; AREA POSTREMA; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; FLOW CYTOMETRY; LEUKOCYTES; MACROPHAGE ACTIVATION; MALE; MICROGLIA; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, TRKA; STRESS, PSYCHOLOGICAL;

EID: 84939561960     PISSN: 10217401     EISSN: 14230216     Source Type: Journal    
DOI: 10.1159/000369350     Document Type: Article

References (55)

1. Salim S, Chugh G, Asghar M: Inflammation in anxiety. Adv Protein Chem Struct Biol 2012; 88: 1-25.
2. Garcia-Bueno B, Caso JR, Leza JC: Stress as a neuroinflammatory condition in brain: damaging and protective mechanisms. Neurosci Biobehav Rev 2008; 32: 1136-1151.
3. Ziemssen T, Kern S: Psychoneuroimmunology - cross-talk between the immune and nervous systems. J Neurol 2007; 254(suppl 2):II8-II11.
4. Jurgens HA, Johnson RW: Dysregulated neuronal- microglial cross-talk during aging, stress and inflammation. Exp Neurol 2012; 233: 40-48.
5. Tynan RJ, Naicker S, Hinwood M, Nalivaiko E, Buller KM, Pow DV, Day TA, Walker FR: Chronic stress alters the density and morphology of microglia in a subset of stress-responsive brain regions. Brain Behav Immun 2010; 24: 1058-1068.
6. London A, Cohen M, Schwartz M: Microglia and monocyte-derived macrophages: functionally distinct populations that act in concert in CNS plasticity and repair. Front Cell Neurosci 2013; 7: 34.
7. Wohleb ES, McKim DB, Shea DT, Powell ND, Tarr AJ, Sheridan JF, Godbout JP: Re-establishment of anxiety in stress-sensitized mice is caused by monocyte trafficking from the spleen to the brain. Biol Psychiatry 2014; 75: 970-981.
8. Wohleb ES, Powell ND, Godbout JP, Sheridan JF: Stress-induced recruitment of bone marrow-derived monocytes to the brain promotes anxiety-like behavior. J Neurosci 2013; 33: 13820-13833.
9. Maolood N, Meister B: Protein components of the blood-brain barrier (BBB) in the brainstem area postrema-nucleus tractus solitarius region. J Chem Neuroanat 2009; 37: 182-195.
10. Fry M, Ferguson AV: The sensory circumventricular organs: brain targets for circulating signals controlling ingestive behavior. Physiol Behav 2007; 91: 413-423.
11. Cottrell GT, Ferguson AV: Sensory circumventricular organs: central roles in integrated autonomic regulation. Regul Pept 2004; 117: 11-23.
12. Roth J, Harre EM, Rummel C, Gerstberger R, Hubschle T: Signaling the brain in systemic inflammation: role of sensory circumventricular organs. Front Biosci 2004; 9: 290-300.
13. Rummel C, Inoue W, Poole S, Luheshi GN: Leptin regulates leukocyte recruitment into the brain following systemic LPS-induced inflammation. Mol Psychiatry 2010; 15: 523-534.
14. Goehler LE, Erisir A, Gaykema RP: Neuralimmune interface in the rat area postrema. Neuroscience 2006; 140: 1415-1434.
15. Schmitt C, Strazielle N, Ghersi-Egea JF: Brain leukocyte infiltration initiated by peripheral inflammation or experimental autoimmune encephalomyelitis occurs through pathways connected to the CSF-filled compartments of the forebrain and midbrain. J Neuroinflammation 2012; 9: 187.
16. Schulz M, Engelhardt B: The circumventricular organs participate in the immunopathogenesis of experimental autoimmune encephalomyelitis. Cerebrospinal Fluid Res 2005; 2: 8.
17. Ziegler DR, Herman JP: Neurocircuitry of stress integration: anatomical pathways regulating the hypothalamo-pituitary-adrenocortical axis of the rat. Integr Comp Biol 2002; 42: 541-551.
18. Liang NC, Smith ME, Moran TH: Palatable food avoidance and acceptance learning with different stressors in female rats. Neuroscience 2013; 235: 149-158.
19. Vargas-Caraveo A, Castillo-Michel H, Mejia- Carmona GE, Perez-Ishiwara DG, Cotte M, Martinez-Martinez A: Preliminary studies of the effects of psychological stress on circulating lymphocytes analyzed by synchrotron radiation based-Fourier transform infrared microspectroscopy. Spectrochim Acta A Mol Biomol Spectrosc 2014; 128: 141-146.
20. Dielenberg RA, McGregor IS: Defensive behavior in rats towards predatory odors: a review. Neurosci Biobehav Rev 2001; 25: 597-609.
21. Paxinos G, Watson C: The Rat Brain in Stereotaxic Coordinates. San Diego, Academic Press, 2006.
22. Walker FR, Beynon SB, Jones KA, Zhao Z, Kongsui R, Cairns M, Nilsson M: Dynamic structural remodelling of microglia in health and disease: a review of the models, the signals and the mechanisms. Brain Behav Immun 2014; 37: 1-14.
23. Marques CP, Cheeran MC, Palmquist JM, Hu S, Urban SL, Lokensgard JR: Prolonged microglial cell activation and lymphocyte infiltration following experimental herpes encephalitis. J Immunol 2008; 181: 6417-6426.
24. Van Loo G, De Lorenzi R, Schmidt H, Huth M, Mildner A, Schmidt-Supprian M, Lassmann H, Prinz MR, Pasparakis M: Inhibition of transcription factor NF-kappaB in the central nervous system ameliorates autoimmune encephalomyelitis in mice. Nat Immunol 2006; 7: 954-961.
25. Price CJ, Hoyda TD, Ferguson AV: The area postrema: a brain monitor and integrator of systemic autonomic state. Neuroscientist 2008; 14: 182-194.
26. Krisch B, Leonhardt H, Buchheim W: The functional and structural border between the CSF- and blood-milieu in the circumventricular organs (organum vasculosum laminae terminalis, subfornical organ, area postrema) of the rat. Cell Tissue Res 1978; 195: 485-497.
27. Dustin ML: Signaling at neuro/immune synapses. J Clin Invest 2012; 122: 1149-1155.
28. Bush TG, Puvanachandra N, Horner CH, Polito A, Ostenfeld T, Svendsen CN, Mucke L, Johnson MH, Sofroniew MV: Leukocyte infiltration, neuronal degeneration, and neurite outgrowth after ablation of scar-forming, reactive astrocytes in adult transgenic mice. Neuron 1999; 23: 297-308.
29. Wang DB, Dayton RD, Henning PP, Cain CD, Zhao LR, Schrott LM, Orchard EA, Knight DS, Klein RL: Expansive gene transfer in the rat CNS rapidly produces amyotrophic lateral sclerosis relevant sequelae when TDP-43 is overexpressed. Mol Ther 2010; 18: 2064-2074.
30. Bentivoglio M, Mariotti R, Bertini G: Neuroinflammation and brain infections: historical context and current perspectives. Brain Res Rev 2011; 66: 152-173.
31. Hickey WF: Leukocyte traffic in the central nervous system: the participants and their roles. Semin Immunol 1999; 11: 125-137.
32. Huitinga I, van Rooijen N, de Groot CJ, Uitdehaag BM, Dijkstra CD: Suppression of experimental allergic encephalomyelitis in Lewis rats after elimination of macrophages. J Exp Med 1990; 172: 1025-1033.
33. Djukic M, Mildner A, Schmidt H, Czesnik D, Bruck W, Priller J, Nau R, Prinz M: Circulating monocytes engraft in the brain, differentiate into microglia and contribute to the pathology following meningitis in mice. Brain 2006; 129: 2394-2403.
34. Varvel NH, Grathwohl SA, Baumann F, Liebig C, Bosch A, Brawek B, Thal DR, Charo IF, Heppner FL, Aguzzi A, Garaschuk O, Ransohoff RM, Jucker M: Microglial repopulation model reveals a robust homeostatic process for replacing CNS myeloid cells. Proc Natl Acad Sci USA 2012; 109: 18150-18155.
35. Simard AR, Rivest S: Bone marrow stem cells have the ability to populate the entire central nervous system into fully differentiated parenchymal microglia. FASEB J 2004; 18: 998-1000.
36. Schwartz M, Baruch K: The resolution of neuroinflammation in neurodegeneration: leukocyte recruitment via the choroid plexus. EMBO J 2014; 33: 7-22.
37. Schwartz M, Kipnis J: A conceptual revolution in the relationships between the brain and immunity. Brain Behav Immun 2011; 25: 817-819.
38. Hinwood M, Morandini J, Day TA, Walker FR: Evidence that microglia mediate the neurobiological effects of chronic psychological stress on the medial prefrontal cortex. Cereb Cortex 2012; 22: 1442-1454.
39. Beumer W, Gibney SM, Drexhage RC, Pont- Lezica L, Doorduin J, Klein HC, Steiner J, Connor TJ, Harkin A, Versnel MA, Drexhage HA: The immune theory of psychiatric diseases: a key role for activated microglia and circulating monocytes. J Leukoc Biol 2012; 92: 959-975.
40. Lewitus GM, Cohen H, Schwartz M: Reducing post-traumatic anxiety by immunization. Brain Behav Immun 2008; 22: 1108-1114.
41. Muldoon LL, Alvarez JI, Begley DJ, Boado RJ, Del Zoppo GJ, Doolittle ND, Engelhardt B, Hallenbeck JM, Lonser RR, Ohlfest JR, Prat A, Scarpa M, Smeyne RJ, Drewes LR, Neuwelt EA: Immunologic privilege in the central nervous system and the blood-brain barrier. J Cereb Blood Flow Metab 2013; 33: 13-21.
42. Holtzman DM, Kilbridge J, Li Y, Cunningham ET Jr, Lenn NJ, Clary DO, Reichardt LF, Mobley WC: TrkA expression in the CNS: evidence for the existence of several novel NGF-responsive CNS neurons. J Neurosci 1995; 15: 1567-1576.
43. Arredondo LR, Deng C, Ratts RB, Lovett- Racke AE, Holtzman DM, Racke MK: Role of nerve growth factor in experimental autoimmune encephalomyelitis. Eur J Immunol 2001; 31: 625-633.
44. Caroleo MC, Costa N, Bracci-Laudiero L, Aloe L: Human monocyte/macrophages activate by exposure to LPS overexpress NGF and NGF receptors. J Neuroimmunol 2001; 113: 193-201.
45. Aloe L, Alleva E, Fiore M: Stress and nerve growth factor: findings in animal models and humans. Pharmacol Biochem Behav 2002; 73: 159-166.
46. Hadjiconstantinou M, McGuire L, Duchemin AM, Laskowski B, Kiecolt-Glaser J, Glaser R: Changes in plasma nerve growth factor levels in older adults associated with chronic stress. J Neuroimmunol 2001; 116: 102-106.
47. El Zein N, D'Hondt S, Sariban E: Crosstalks between the receptors tyrosine kinase EGFR and TrkA and the GPCR, FPR, in human monocytes are essential for receptors-mediated cell activation. Cell Signal 2010; 22: 1437-1447.
48. Gladkevich A, Kauffman HF, Korf J: Lymphocytes as a neural probe: potential for studying psychiatric disorders. Prog Neuropsychopharmacol Biol Psychiatry 2004; 28: 559-576.
49. la Sala A, Corinti S, Federici M, Saragovi HU, Girolomoni G: Ligand activation of nerve growth factor receptor TrkA protects monocytes from apoptosis. J Leukoc Biol 2000; 68: 104-110.
50. De Simone R, Ambrosini E, Carnevale D, Ajmone- Cat MA, Minghetti L: NGF promotes microglial migration through the activation of its high affinity receptor: modulation by TGF-beta. J Neuroimmunol 2007; 190: 53-60.
51. Shechter R, Miller O, Yovel G, Rosenzweig N, London A, Ruckh J, Kim KW, Klein E, Kalchenko V, Bendel P, Lira SA, Jung S, Schwartz M: Recruitment of beneficial M2 macrophages to injured spinal cord is orchestrated by remote brain choroid plexus. Immunity 2013; 38: 555-569.
52. Valcour VG, Shiramizu BT, Shikuma CM: HIV DNA in circulating monocytes as a mechanism to dementia and other HIV complications. J Leukoc Biol 2010; 87: 621-626.
53. Fuchs F, Damm J, Gerstberger R, Roth J, Rummel C: Activation of the inflammatory transcription factor nuclear factor interleukin-6 during inflammatory and psychological stress in the brain. J Neuroinflammation 2013; 10: 140.
54. Franceschi C, Bonafe M, Valensin S, Olivieri F, De Luca M, Ottaviani E, De Benedictis G: Inflamm-aging. An evolutionary perspective on immunosenescence. Ann NY Acad Sci 2000; 908: 244-254.
55. Ottaviani E, Franceschi C: The neuroimmunology of stress from invertebrates to man. Prog Neurobiol 1996; 48: 421-440.